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Quercus species divergence is driven by natural selection on evolutionarily less integrated traits.

ABSTRACT: Functional traits are organismal attributes that can respond to environmental cues, thereby providing important ecological functions. In addition, an organism's potential for adaptation is defined by the patterns of covariation among groups of functionally related traits. Whether an organism is evolutionarily constrained or has the potential for adaptation is based on the phenotypic integration or modularity of these traits. Here, we revisited leaf morphology in two European sympatric white oaks (Quercus petraea (Matt.) Liebl. and Quercus robur L.), sampling 2098 individuals, across much of their geographical distribution ranges. At the phenotypic level, leaf morphology traditionally encompasses discriminant attributes among different oak species. Here, we estimated in situ heritability, genetic correlation, and integration across such attributes. Also, we performed Selection Response Decomposition to test these traits for potential differences in oak species' evolutionary responses. Based on the uncovered functional units of traits (modules) in our study, the morphological module "leaf size gradient" was highlighted among functionally integrated traits. Equally, this module was defined in both oaks as being under "global regulation" in vegetative bud establishment and development. Lamina basal shape and intercalary veins' number were not, or, less integrated within the initially defined leaf functional unit, suggesting more than one module within the leaf traits' ensemble. Since these traits generally show the greatest species discriminatory power, they potentially underwent effective differential response to selection among oaks. Indeed, the selection of these traits could have driven the ecological preferences between the two sympatric oaks growing under different microclimates.

SUBMITTER: Klapste J

PROVIDER: S-EPMC8027598 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:A major goal in evolutionary biology is to understand how natural selection has shaped patterns of genetic variation across genomes. Studies in a variety of species have shown that neutral genetic diversity (intra-species differences) has been reduced at sites linked to those under direct selection. However, the effect of linked selection on neutral sequence divergence (inter-species differences) remains ambiguous. While empirical studies have reported correlations between divergence and recombination, which is interpreted as evidence for natural selection reducing linked neutral divergence, theory argues otherwise, especially for species that have diverged long ago. Here we address these outstanding issues by examining whether natural selection can affect divergence between both closely and distantly related species. We show that neutral divergence between closely related species (e.g. human-primate) is negatively correlated with functional content and positively correlated with human recombination rate. We also find that neutral divergence between distantly related species (e.g. human-rodent) is negatively correlated with functional content and positively correlated with estimates of background selection from primates. These patterns persist after accounting for the confounding factors of hypermutable CpG sites, GC content, and biased gene conversion. Coalescent models indicate that even when the contribution of ancestral polymorphism to divergence is small, background selection in the ancestral population can still explain a large proportion of the variance in divergence across the genome, generating the observed correlations. Our findings reveal that, contrary to previous intuition, natural selection can indirectly affect linked neutral divergence between both closely and distantly related species. Though we cannot formally exclude the possibility that the direct effects of purifying selection drive some of these patterns, such a scenario would be possible only if more of the genome is under purifying selection than currently believed. Our work has implications for understanding the evolution of genomes and interpreting patterns of genetic variation.

Project description:Long-distance dispersal (LDD) outside a species' breeding range contributes to genetic divergence. Previous phylogeographic studies of migratory bird species have not discriminated LDD from vicariant speciation in their diversification process. We conducted an integrative phylogeographic approach to test the LDD hypothesis, which predicts that a Japanese migratory bird subspecies diverged from a population in the coastal region of the East China Sea (CRECS) via LDD over the East China Sea (ECS). Haplotype networks of both mitochondrial and nuclear genes of its three subspecies were reconstructed to examine whether the Japanese subspecies of the Brown Shrike (Lanius cristatus superciliosus) diverged from an ancestral CRECS population. A species distribution model (SDM) for the Japanese subspecies was constructed using bioclimatic variables under the maximum entropy algorithm. It was projected backwards to the climate of the last glacial maximum (LGM) to infer the candidate source area of colonization. A migratory route of L. c. superciliosus, which possibly reflects a candidate past colonization route, was tracked by light-level geolocators. Molecular phylogenetic networks suggest that the Japanese subspecies diverged from a population in the CRECS and maintained anciently diverged haplotypes. The SDM inferred that the emerged continental shelf of the ECS and the present CRECS were suitable breeding areas for the Japanese subspecies during the LGM. A major migratory route for L. c. superciliosus was inferred between the CRECS and the Japanese archipelago across the ECS. Our integrative approach supported the LDD hypothesis for divergence of the Japanese subspecies of the Brown Shrike. Shrinkage of the ECS may have been responsible for successful population establishment, due to a sufficient number of migrants overshooting to the Japanese archipelago from the CRECS. Our framework provides a new phylogeographic scenario for this region. Discriminating LDD and vicariance models helps improve our understanding of the phylogeographic histories of migratory species.

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Quercus species divergence is driven by natural selection on evolutionarily less integrated traits.

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